Representing Spatial Information for Limb Movement: Role of Area 5 in the Monkey

“Area PMd also receives direct visual (Caminiti et al., 1996) and higher-level proprioceptive (Lacquaniti et al., 1995) input from the SPL. Somatosensory information concerning limb position is provided to PMd via a circuit interconnecting PEc/PEip-F2 (Matelli et al., 1998).”

“The relative magnitudes of the enhancing and suppressing effects of attention on neural activity in parietal cortex may vary as a function of parietal subdivision and task paradigm; however, both effects substantiate the involvement of PPC in the control of spatial attention at the cellular level.”

“The superior parietal lobule also codes the location of body parts in a body-centered coordinate system as well as the location of objects in space thus establishing the relative location of objects to the body (see e.g., Duffy and Burchfiel 1971; Lacquaniti et al. 1995; Mountcastle et al. 1975; Sakata et al. 1973).”

“…regions; Temp Vis, temporal visual areas. somatic neurons in the posterior parietal cortex of the monkey are responsive to passive stimulation (Lacquaniti et al., 1995); thus, in our preparation we may have been recording from clusters of passively responsive Class II type visual and/or…”

“There exist some important features which differentiate the behaviour of neurones in parietal area 5 (Lacquaniti et al., 1995) and areas”

“However, referring to an early report by Delay (1935), Mauguiere et al. (1983) proposed that astereognosis might represent a more complex perceptual disorder, i.”

“Specific evidence for egocentric representations of endpoint position during reaching toward visual targets has been provided by a study of the superior parietal lobule of the monkey ( Lacquaniti et al. 1995 ).”

“SPL is activated by movements in extrapersonal space relative to a proprioceptive reference frame (Roland et al. 1980) and represents spatial information for limb movement (Lacquaniti et al. 1995).”

“Target location and movement direction can be defined in eye-centered, armcentered or object-centered coordinates depending on the cerebral area and the task (Batista et al. 1999; Caminiti et al. 1990; Fogassi et al. 1996; Lacquaniti et al. 1995; Tremblay et al. 2002).”

“It in the integration of the spatial components of movement (Andersen, 1995; Lacquaniti et al., 1995).”

“…1984; Caminiti et al., 1990; Prud’homme and Kalaska, 1994; Lacquaniti et al., 1995), direction (Georgopoulos et al., 1981; Caminiti et al., 1990; Lacquaniti et al., 1995), amplitude (Fu et al., 1993), velocity (Ashe and Georgopoulos, 1994; Moran and Schwartz, 1999; Averbeck et al., 2005;…”

“logical recordings of the macaque demonstrating its role in the manipulation of objects in space (Sakata et al., 1973; Mountcastle et al., 1975; Taira et al., 1990; Lacquaniti et al., 1995; Georgopoulos et al., 2005).”

“It remains debatable how these signals are converted to perceive arm position and aid movement control (Flanders et al. 1992; Scott and Loeb 1994; Lacquaniti et al. 1995; Scott et al. 1997) .”

“Our work focuses on the motor cortex; however, it is well known that limb movement is also encoded in other cortical areas, such as the parietal cortex (Lacquaniti et al. 1995).”

“Most of the neurophysiological studies that so far have investigated reaching in 3D space (Schwartz et al., 1988; Caminiti et al., 1990, 1991; Ferraina and Bianchi 1994; Lacquaniti et al., 1995; Johnson et al., 1996; Taira et al., 1996; Fattori et al., 2005, 2009) either explored only two depth planes or did not contr…”

“However, the presence in area 5 of cells tuned to the location of visual targets in a shoulder-centered frame of reference (Lacquaniti et al., 1995) suggests that the spatial coding postulated by the target position hypothesis may be implemented in the parietal cortex.”

“, 1991), and parietal area 5 (Lacquaniti et al., 1995), 3D arm reaching is encoded in shoulder-centered coordinates.”

“To our knowledge, only Lacquaniti et al. (1995) who studied this issue in the macaque posterior parietal cortex (PPC) reported distinct subpopulations of neurons in area PE representing the distance, azimuth, and elevation of target location.”

“Furthermore, Area 5 uses more body- or hand-centered representations compared to the eye-centered representations reported in MIP (Batista et al., 1999; Buneo et al., 2002; Chang and Snyder, 2010; Colby and Duhamel, 1996; Ferraina et al., 2009; Kalaska, 1996; Lacquaniti et al., 1995; Marconi et al., 2001; Scott et al.…”

“the PePV, ReVV, TPV, and DV (in area 5, cf. Lacquaniti et al., 1995), as well as the MIV (in area 4), operate in shoulder-centered coordinates.”

“There is recent evidence that dorsal area 5 (area PE) might be a substrate for egocentric representations of reaching in the monkey (Lacquaniti et al. 1995; Lacquaniti 1997; Lacquaniti and Caminiti 1998).”

“Neurons in the superior parietal lobe are active during passive joint rotation and deep tissue pressure as well as during active arm movements (Mountcastle et al., 1975; Lacquaniti et al., 1995).”

“Monkey area PE, the area forming most of the superior parietal lobe convexity, has been shown to be active during passive joint rotation, deep tissue pressure, and active arm movements (Sakata et al. 1973; Mountcastle et al. 1975; Lacquaniti et al. 1995).”

“However, the constant pattern of trajectory curvature observed after SPL inactivation raises the possibility that the impaired performance can be a consequence of the breakdown in the transformation of the desired hand-path into a sequence of appropriate joint rotations and/or in the control of the posture and geometr…”

“SPL is known to code body part location information in a body-centered coordinate system and to establish the relative location of objects with respect to the body (e.g., Duffy and Burchfiel 1971; Lacquaniti et al. 1995; Mountcastle et al. 1975; Sakata et al. 1973) indicating STG(MdLF)SPL’s role in visuospatial attent…”

“…Costanzo, 1981; Cohen et al., 1994; Prud'homme and Kalaska, 1994; Helms Tillery et al., 1996), anterior parietal cortex (Kalaska et al., 1983; Lacquaniti et al., 1995), motor cortex (Kettner et al., 1988; Caminiti et al., 1990) and premotor cortex (Caminiti et al., 1991), but also earlier…”

“…Vector signal is based upon their tuning to movement direction, onset timing, and primability (Burbaud, Doegle, Gross, & Bioulac, 1991; Chapman, Spidalieri, & Lamarre, 1984; Crammond & Kalaska, 1989; Kalaska, Cohen, Prud’homme, & Hyde, 1990; Lacquaniti, Guigon, Bianchi, Ferraina, & Caminiti, 1995).”

“…have confirmed that area 5 neurons are involved in the preparation of movement (Burbaud et al., 1991) and in generating body-, shoulder-, or hand-center coordinates for reaching (Ferraina and Bianchi, 1994; Lacquaniti et al., 1995; Kalaska, 1996; Graziano et al., 2000; Bremner and Andersen, 2012).”

“In this light, endpoint–position sensitive neurons, such as those found in parietal cortex area 5, become good candidates for the locus of the target position memory (Lacquaniti et al., 1995).”

“More recently, Lacquaniti et al. (1995) have demonstrated that variations in the activities of neurons in parietal area 5 during the maintenance of various static arm postures can be described quite well in a body-fixed frame of reference, the coordinates of which include the azimuth, elevation,…”

“It should be noted that JD’s lesion site is consistent with electrophysiological investigations in monkeys documenting the role of neurons in area 5 in coding static positions of the hand and target locations in intrinsic egocentric coordinates (Lacquaniti et al., 1995).”

“Furthermore, information can be encoded in different coordinate systems; for example, the visual modality could encode the distance between object and eye in Cartesian (or polar) coordinates, centered at the eye or at other body’s parts (Lacquaniti et al., 1995).”

“3) could indicate a specialization of this region for the processing of spatial relationships between the limbs and objects in extrapersonal space (Connolly et al. 2003; Johnson et al. 1996; Lacquaniti et al. 1995; Roland et al. 1980).”

“2009), and the coordinate transformation of reach targets into body- and shoulder-centered coordinates (Ferraina and Bianchi 1994; Lacquaniti et al. 1995; Seelke et al. 2012).”

“For example, neurons in the superior parietal lobule (SPL), dorsal (PMd) and ventral (PMv) premotor cortex, and primary motor cortex (M1) represent the target’s spatial location, although in M1, this information is strongly linked to movement execution (Lacquaniti et al., 1995; Shen and Alexander, 1997a, 1997b).”

“…to task factors including delay periods (Crammond and Kalaska 1989), dynamics (Kalaska et al. 1990), different periods of a delayed reach task (Johnson et al. 1996), and movements made in a similar direction but within different parts of space (Ferraina and Bianchi 1994; Lacquaniti et al. 1995).”

“This information is further processed in the posterior parietal cortex, as well as Brodmann’s area 7 for visualproprioceptive integration [Andersen, 1997; Lacquaniti et al., 1995].”

“Nevertheless, other studies have also described strong quantitative correlations of area 5 activity with a variety of parameters of the spatiotemporal kinematics of arm movements, such as direction, velocity, and current and intended arm positions (Andersen & Buneo 2003; Ashe & Georgopoulos 1994; Buneo et al 2002; Kal…”

“…that a substantial number of neurons in this study were modulated by eye and/or limb position signals, consistent with previous findings in the superior parietal lobule (Chang et al. 2009; Cisek and Kalaska 2002; Ferraina et al. 2009; Johnson et al. 1996; Lacquaniti et al. 1995; Scott et al. 1997).”

“…showed that area PE, located rostrally to PEc, containsmostly cells representing reach targets in hand-centered coordinates (Ferraina et al. 2009; Bremner and Andersen 2012), together with body-centered cells (Lacquaniti et al. 1995; Buneo et al. 2002) and “mixed” cells (McGuire and Sabes 2011).”

“…motion; visuomotor integration; macaque monkey Monkey’s area PE (Brodmann’s area 5), classically known as a somatic sensorimotor association area, has been suggested to be involved in egocentric representation of reaching in the monkey (for review, see Lacquaniti et al., 1995; Kalaska, 1996).”

“In confirmation of this ex- and the target position of a reach (Lacquaniti et al. 1995).”

“However, studies of cell activity in motor, premotor and superior parietal cortex have consistently shown that neural activity is highly correlated to the direction of hand movement within a high-order reference frame, although in a way that depends on a variety of factors, including the starting hand position (Camini…”

“, 1990) and the location of the arm in space in a body-centred coordinate system (Lacquaniti et al., 1995).”

“Third, Bullock et al. (1998) extended the VITE model to provide an account for load-sensitive and load-insensitive directional tuning in the cortical areas four and five (e.g. Georgopoulos et al. 1982; Kalaska et al. 1989, 1990; Lacquaniti et al. 1995).”

“…start locations, and goal locations are all represented in motor planning areas and any or all of these features could be remapped during motor adaptation (Graziano et al., 1994; Lacquaniti et al., 1995; Duhamel et al., Received Aug. 6, 2012; revised March 11, 2013; accepted April 10, 2013.”

“It was initially suggested that this transformation takes place serially in PPC, that is, caudal PPC areas encode reach targets in eye-centered RF, whereas the rostral ones use handcentered coordinates (Lacquaniti et al. 1995; Batista et al. 1999; Buneo et al. 2002, 2008; Marzocchi et al. 2008).”

“In humans as well as in monkeys, the superior parietal lobule and adjacent area 2 belong to the dorso-dorsal pathway (Rizzolatti and Matelli 2003) which integrates spatial limb representations with physical object features to create appropriate motor commands for grasping and reaching (Daprati and Sirigu 2006; Buxbaum…”

“Studies of dorsal area 5 (area 5d), which lies adjacent to MIP, have also clearly pointed to a strong influence of postural information in cell discharge (Lacquaniti et al., 1995; Scott et al., 1997), and activity starts to increase until the effector is unambiguously specified as arm (Cui and Andersen, 2011).”

“Indeed, recent work has shown that neurons of area 5 in the posterior parietal cortex can encode hand position relative to the body in a spherical coordinate system with a vertical axis ( Lacquaniti et al. 1995 ).”

“A large number of experiments in both human and non-human primates corroborated the view that two separate pathways, connecting the posterior parietal cortex (PPC) to the premotor cortex, subserve the two movement components underlying prehension, allowing primates to interact so skillfully with their environment (Jea…”

“…similar conclusions were drawn from the results of an earlier reaching study in which the activity of subsets of area 5 neurons was observed to be related to the initial or upcoming position of the limb (Lacquaniti et al., 1995), though eye position was not controlled or monitored in that study.”

“In order to control movement of limbs and other body parts, area 4 is thought to integrate information from area 5 on the spatial location of the body parts (Lacquaniti et al., 1995).”

“Such results indicate that synergies serve the implementation of a few global movement features like movement direction and amplitude which are coded by independent neuronal populations in the brain (35).”